A little winning streak: The reptilian‐eye view of gastrulation in birds

Abstract

The primitive streak is where the mesoderm and definitive endoderm precursor cells ingress from the epiblast during gastrulation. It is often described as an embryological feature common to all amniotes. But such a feature has not been associated with gastrulation in any reptilian species. A parsimonious model would be that the primitive streak evolved independently in the avian and mammalian lineages. Looking beyond the primitive streak, can one find shared features of mesoderm and endoderm formation during amniote gastrulation? Here, we survey the literature on reptilian gastrulation and provide new data on Brachyury RNA and laminin protein expression in gastrula-stage turtle (Pelodiscus sinensis) embryos. We propose a model to reconcile the primitive streak-associated gastrulation in birds and the blastopore-associated gastrulation in extant reptiles.

Decoupling of amniote gastrulation and streak formation reveals a morphogenetic unity in vertebrate mesoderm induction

“…4A,B). Embryos of the Chinese softshelled turtle (Pelodiscus sinensis), a reptilian species that does not form a streak in its early development (Bertocchini et al, 2013;…”

“…The evolutionary origin of the streak has long been debated and its relationship to the blastopore remains unresolved. The reptiles, the stem amniote lineage from which both the mammals and birds evolved, do not have a streak (Bertocchini et al, 2013). Furthermore, mammals and birds have been hypothesized to employ different cellular mechanisms to generate a streak (Arnold and Robertson, 2009;Chuai and Weijer, 2008;Stern, 2004;Voiculescu et al, 2007;Williams et al, 2012).…”

On the Enigma of the Human Neurenteric Canal

“…DOI: 10.1159/000493276 the blastopore with its adjacent blastoporal lips in amphibia: both the neurenteric canal and the blastopore are in their cranial part associated with an involution-type cell movement for the formation of the notochordal plate, and this shows striking parallels in primates [this study], bats [van Beneden, 1888], reptiles [Bertocchini et al, 2013;Stower and Bertocchini, 2017], amphibia [Shook and Keller, 2008], and in a number of bird species (including the chick: Charrier et al [1999]; Tsikolia et al [2012]), some of which may also have a notochordal canal ("rudimentary Urdarm") or even a true neurenteric canal [Schauins land, 1903]; in the chick, however, a neurenteric canal next to the HINC-like cellular arrangement within the primitive node [Tsikolia et al, 2012] has not yet been reported. The primitive streak itself would, hence, represent a homologue of the lateral and ventral parts of the blastopore as described before (see Hertwig [1906] and references therein).…”

“…Blastopore and primitive streak have, therefore, repeatedly presented to be functional equivalents derived from a common ancestor and thus to be homologous structures [Arendt and Nübler-Jung, 1999]. A recent focus on reptiles, however, led to the proposal that the avian and the human primitive streak may have developed independently and that reptiles with their narrow canal-like blastopore, which runs more or less perpendicularly through the embryonic plate connecting the amniotic cavity with the yolk sac cavity [Bertocchini et al, 2013], may have an "intermediate blastopore" or "proto-streak" with crucial importance for gastrulation [Stower and Bertocchini, 2017].…”

Taking the Middle Road

“…In support of this line of thinking, two recent papers from Guojun Sheng and colleagues suggest that the switch between circular and linear internalization architecture is more facile than might have been imagined. The first paper documents reptilian species in which mesendoderm internalization occurs through a blastopore-like region and involves a combination of involution and ingression (Bertocchini et al, 2013). Since birds are evolutionarily closer to reptiles than mammals, this observation suggests an instance of convergent evolution whereby avian and mammalian primitive streaks independently evolved from an ancestral blastopore-like configuration.…”